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Home , Acouchi, Agouti, Astrocaryum standleyanum, Black agouti, Central American agouti, Dasyproctidae

Determinants for the Diet of Captive (Dasyprocta spp.)

a,b, Deborah A. McWilliams, MSc *

KEYWORDS  Dasyprocta  Diet  Rodentia   Captive  Nutrition  Frugivore  Omnivore

Sparse attention in the literature has been given to the considerations for an appro- priate, practical diet for captive of the Dasyprocta (order Rodentia, family , common name agouti). Dasyprocta includes 11 extant distributed throughout , , and some associated islands (Coiba Island , Roatan Island Honduras, and the Lesser Antilles). The species name, common name and average weights of the species in this genus are listed in Table 1.1,2 These species are terrestrial that prefer neotropical savannas and evergreen forests.3,4 All species of Dasyprocta are diurnal5 and are classified as scatter-hoarding frugivores.6–9 Current species holdings in zoos that participate in the International Species Information System (ISIS) include Dasyprocta azarae, D cris- tata, D fuliginosa, D leporine (and subspecies), D mexicana, D prymnolopha, and D punctata (and subspecies).10 Species in the genus Dasyprocta resemble but they are larger and more slender.11 Dasyprocta are not burrowers,8,11,12 although they use crevices or existing burrows for birthing and raising pups.11–13

DIET CLASSIFICATION There is much evidence supporting classification of Dasyprocta species as a frugi- vore.6–9 For example, D leporine is reported to have a wild diet that is 87% fruit, 6% matter, 4% fibrous foods, and 2% leaves.8,9 There is an equal—if not over- whelming—amount of evidence that species of Dasyprocta are omnivores, however. Dasyprocta, as members of the order Rodentia, have the generalist feeder, dentition to support an omnivorous adaptation.14 Similar to most caviomorphs, the

a American Association of Zoos and Aquariums Rodent, Insectivore and Lagomorph Taxon Advisory Group (AZA RIL-TAG), USA b Canadian Association of Zoos and Aquariums Nutrition Advisory Group (CAZA-NARG), 807-40 Vanier Drive, Guelph, ON, N1G 2X7 Canada * Canadian Association of Zoos and Aquariums Nutrition Advisory Group (CAZA-NARG), 807-40 Vanier Drive, Guelph, ON, N1G 2X7 Canada. E-mail address: [email protected]

Vet Clin Exot Anim 12 (2009) 279–286 doi:10.1016/j.cvex.2009.01.001 vetexotic.theclinics.com 1094-9194/09/$ – see front matter ª 2009 Elsevier Inc. All rights reserved. 280 McWilliams

Table 1 Species name, common name, and average weights of species in the genus Dasyprocta

Species Common Name AverageWeight (kg) Dasyprocta azarae Azara’s agouti 2.711 2–41 3.82 Dasyprocta coibae Coiban agouti — Dasyprocta cristata Crested agouti — Dasyprocta fuliginosaa 3.5–65 2.711 Dasyprocta guamara Orinoco agouti — Dasyprocta kalinowskii Kalinowski’s agouti — Dasyprocta leporinaa Brazilian agouti or 3.0–5.913 orange-rumped agouti 2.72,6,11 4.0–5.88 Dasyprocta mexicana Mexican agouti 2.0–4.05 Dasyprocta prymnolopha Black-rumped agouti 3.1–4 kg11 Dasyprocta punctataa Central-American agouti 3.0–5.25 3.1–411 2–41,27 Dasyprocta ruatanica Ruatan Island agouti —

a There are subspecies.

dental formula of Dasyprocta species is I 1/1, C 0/0, P 1/1, M 3/3.11 The incisors are continuously growing with restricted enamel on the anteroventral surface that is resis- tant to compressive strain and has a sharp edge for shaving and chiseling.14 The jaw can move forward and create two occlusions: the incisors occlude (for gnawing and chiseling) but the cheek teeth do not, or the cheek teeth occlude (for mastication) and the incisors do not. When the incisors are occluded and used for chiseling nonfood items, the skin of the upper lip can close off the mouth cavity to prevent entry of nonfood material. In general, the upper incisors can cut vegetation and pierce inver- tebrates or the flesh of vertebrates, and the lower incisors can cut and shear food, including flesh. The cheek teeth are used for grinding and chewing foods, including animal and foods. Further support for classification of Dasyprocta species as omnivores is the denti- tion wear patterns described in wild caviomorph rodents. In one study, a lack of distinctive wear patterns prevented diet specialization classification of wild Dasyprocta as a frugivore, folivore, hard-object specialist, browser, or grazer.15 The dental wear patterns, or lack of patterns, seem to support that these animals are not specialist feeders. Information provided by field studies also supports classification of Dasyprocta species as omnivores. For example, wild Dasyprocta eat: Fruit: citrus fruit and coconuts7,16; avocado, mango, pineapple, tomato, papaya, melon7; Syagrus romanzoffiana (Queen palm, ).4 : leaves,3,9 flowers,3,16 roots.3 Grains: corn, rice.16 Nuts and seeds: fruit seeds,3 almonds,3 standleyanum (black palm) seeds,17 nuts (Bertholletia excelsa),18 dry palm pyrenes (eg, Bactris Determinants for the Diet of Captive Agoutis 281

acanthocarpa, B excelsa, bactris palm),18,19 Hymenaea courbaril L (guapino, locust) seeds,20 Ormosia arborea (Legumindae) and Mimusop coriacea seeds,21 S romanzoffiana.4 Animal Matter: invertebrates.3,9,13,22 Various researchers also report omnivory in Dasyprocta. For example, during the fruit season, Dasyprocta ate a diet of 37% fruit pulp and 44% fruit seeds supple- mented with plant and animal matter. In the off-season, food caches (mostly seeds) and roots were eaten as well as plant and animal matter.3,9,13,17,22 With some variation due to climate and location, fruiting season is from March to June. In addition, there is little to no evidence of dietary specialization in either female or male Dasyprocta. The lack of dietary variation between the sexes in Dasyprocta can probably be attributed to the sharing of territories and common food sources for males and females.9,13,20,23 The evidence supporting omnivory in Dasyprocta species, in general, affects other determinants of dietary requirements in captives.

GASTROINTESTINALTRACT There is a lack of detail describing the physiology of the gastrointestinal tract (GIT) of Dasyprocta species, which might be attributed to the assumption of frugivory and assumptions of homology with species that have been studied, such as the (Cavia porcellus) and the (Agouti paca). These assumptions of frugivory and of homology with other species mean that there is a tendency for literature to rely on existing information for other species. At this time, there is also a lack of any evidence of cecotrophy.

ENDOGENOUS ASCORBIC ACID There is some conflicting evidence for the physiologic ability of Dasyprocta species to endogenously synthesize ascorbic acid. In support of the need for a dietary source of ascorbic acid, the assumption of classification as a frugivore would indicate lack of an evolutionary ability to endogenously create ascorbic acid.7 Captive Dasyprocta seem to preferentially select foods high in ascorbic acid and this may indicate an inability to synthesize ascorbic acid.7 Such an apparent preference may only indicate a prefer- ence for the palatability of those foods higher in ascorbic acid, however (eg, mango, pineapple). Classification as an omnivore supports endogenous ascorbic acid synthesis in Dasyprocta. In addition, because fruits are only available for 4 to 5 months per year, it is questionable how Dasyprocta species obtain sufficient dietary sources of ascorbic acid during the off-season. A study on the biosynthesis of ascorbic acid in the and agouti further supports endogenous ascorbic acid synthesis in Dasyprocta. This study reports that both species have the ability to produce endogenous ascorbic acid.24

SCATTER-HOARDING BEHAVIOR Dasyprocta species are terrestrial scatter-hoarders and various studies report similar caching behavior.8,9,23,25 In general, seeds (and nuts) are cached one at a time after the pulp of a fruit is eaten or discarded8,20,23 and retrieved at some point after the fruit- ing season.9,23 Retrieval can be as long as 8 months after burial.23 Caches are covered with soil and usually a leaf or twig is placed on top after burial in a hole 2 to 8 cm deep.23 282 McWilliams

METABOLIC RATE The metabolic rate of Dasyprocta species varies according to territorial conditions or the housing conditions of captives.16 For example, males bonded to a female are more active and have higher respiration rates and body temperatures (use more energy) than animals housed alone, male/male or all-male groups, or male and female non- bonded pairs. The activity of bonded males seems to be related to territoriality, and behaviors include digging, scrape-marking, and scenting.26 Adult males defend their territory against any male at any time but adult females only defend their territory when food is scarce.11 An equation for estimating basal metabolic rate for Dasyprocta species from 2.7 to 3.3 kg is 8.78 Â weight (kg).27 In general, females weigh more than males.9

APPARENT DIETARY REQUIREMENTS Studies on the captive diets of Dasyprocta are nonexistent. Captive Dasyprocta are reported to eat carrots, potatoes, cassava, and cooked ground beef.23 In general, they eat meat only if cooked but this does not mean they will not eat uncooked flesh. For example, a group of captive Dasyprocta killed and ate an adult male Liomys pictus (painted spiny pocket mouse).23 The high proportion of seeds and nuts in the diets of wild Dasyprocta along with the selection of foods higher in energy and lower in water content in captive animals7 suggest a preference for foods that offer sufficient protein and fats. Protein and fats are minimally available in most fruit pulp.3 For example, avocado is a preferred food of captive Dasyprocta and this fruit is high in protein and fat.7 Dietary fiber levels for wild Dasyprocta seem to be consistent year-round, because of the availability of fruit when in season and the consumption of roots and plant matter during the off-season.9 A suggested level of dietary crude fiber for a 2.7 kg animal is 157 g crude fiber/kg dry matter feed (DM).28 Calculation of dietary fiber levels must be based on fruit without peels, because of the penchant of Dasyprocta to peel fruit before ingestion.23 Captive Dasyprocta seem to prefer foods high in ascorbic acid.7 Again, whether the preference is for the ascorbic acid or the palatable fruit (mango, papaya, melon, oranges, pineapple, and tomato) remains to be determined. Dasyprocta prefer eating either on elevated surfaces or under and within vegetation. They eat by sitting on their haunches and holding food with their forepaws. Food is often examined and tasted before ingestion, and spherical food or objects from 1.5 cm to 15 cm in diameter seem to be the most appealing.23 The practice of handling and tasting food before ingestion is probably a form of examination and determination for suitability as a food. For example, wild Dasyprocta do not eat seeds containing qui- nolizidine alkaloids (QA) although they do cache these seeds.29 QAs can disrupt neural function and they are also a teratogen.21

LIFE STAGE NUTRITION: REPRODUCTION Sexual maturity in Dasyprocta can occur as early as 6 months of age.8 Gestation is approximately 120 days and the precocial pups (one to two) are born furred with their eyes open.11,23,30 Neonates weigh about 22.7 g, and the young are tolerated within a territory even after weaning.23,31 The mating season of wild D punctata is February to April,23 but in captivity D punctata often has two litters per year with about 4 months between litters.8,11 Determinants for the Diet of Captive Agoutis 283

In the wild, pregnant Dasyprocta increase the amount of seeds (protein, fat, and energy) in their diets.3 In captive guinea pigs (Cprocellus), another precocial rodent, the average daily energy intake during gestation was 16% greater than normal intake and energy intake while lactating was 92% greater than normal intake.12 Female agoutis were observed to continue nursing pups as long as 7 weeks post partum.29 As with many species, lactating females should be fed ad lib to guarantee provision of sufficient energy. Despite the precociality of the pups, they will nurse even while eating solid food.12 In the wild, at 1 day old, pups nurse, groom, and search leaf litter.29 The lactating female does not provide the pups with solid food, but the pups do follow her and eat from her foods. Learning is probably a dominant factor in food choice, although pups eventually explore and eat foods not introduced by the dam.29

DIABETES Rodent species have been used for decades as models for human diabetes.31 In addi- tion, wild caviomorph rodents (not including Dasyprocta species) have a low physio- logic activity of insulin (1%–10% of the activity of most ),32 and in serum glucose tests, caviomorph species produced more insulin than most mammals.31 The current hypothesis states that the higher insulin response in these species is a compensatory mechanism for the lower physiologic activity of their insulin.31 This compensatory response may also predispose them to developing diabetes, however.33 Field studies support the hypothesis that a higher insulin response in caviomorph species may predispose them to diabetes. Three wild caviomorph individuals, two Abrocoma bennetti (chinchilla rat) and one Microcavia niata (Andean Mountain cavy), had abnormal serum glucose concentration values and cataracts, and all three animals were obese. These are typical symptoms of diabetes.33 A captive agouti diag- nosed with diabetes was also obese and had cataracts.31 Extrapolating these findings to Dasyprocta species suggests that captives are at extremely high risk for developing diabetes, especially when fed as frugivores. Diabetes in general has become nearly epidemic in captive wild animals. For example, diabetes was once only believed to be a risk factor for sedentary, obese nonhuman primates.34,35 Diabetes is increasingly identified in captive animals of other species, however.36

DENTAL CARIES AND PATHOLOGY Studies of wild Dasyprocta suggest that captives are at high risk for developing dental caries and dental pathology. Dental caries were found in wild populations of cavio- morphs, and this seems related to dietary carbohydrates (mainly those containing fructose, glucose, and sucrose)37,38 that promote plaque and bacteria.39 Dental caries have been induced in laboratory animals by feeding a soft diet high in carbohy- drates.40 In wild populations of caviomorphs, frugivores had the highest incidence of dental caries (10.5%–19.8%) in comparison with grazers (1.1%–8.7%).38 Moderate fresh fruit consumption actually decreases the incidence of dental caries in humans.41

SUMMARY Although there is no existing research on the dietary physiology and nutrition of captive Dasyprocta species, there are several recommendations that can be made for feeding captives. These include:

Feed as omnivores: There is overwhelming evidence that these species are omniv- orous despite a preference for fruit when given food choices. Captive diets 284 McWilliams

should have a high percentage (40% as fed) of foods providing protein and fats (avocado, seeds, nuts, legumes) supplemented with plant matter (40% as fed). Other foods, such as corn, oats, rice, rye, wheat, roots (carrots, parsnips), grasses, leaves, hibiscus flowers, and grains should be fed at about a 10% as-fed level. An estimated dietary crude fiber for a 2.7 kg animal is approxi- mately 157 g crude fiber/kg DM.27 Fruit and insects should be provided as envi- ronmental enrichment at approximately 10% of foods (as fed). Provide opportunities for caching: Scatter-hoarding seems to be an innate behavior of Dasyprocta species. In captivity, caching of food would provide activity at the time of burial and later when food is retrieved. Most exhibits could accommodate an area of dirt of sufficient depth for this activity. Prevent obesity: Caviomorph species are prone to obesity. Vigilant body condition scoring and weighing is the only way to reliably monitor weight gain or loss. In addition, provision for activity, such as caching opportunities, mazes, eleva- tions, burrows, and puzzle boxes with novel items, encourages activity and energy use. Gestation and lactation: The dietary percentage of foods providing protein and fats (seeds, nuts, and so forth) should be increased for gestating females, and the energy content should be increased by at least 16%.12 Food should be provided ad lib for lactating females. Prevent the development of diabetes: Current evidence suggests that wild and captive caviomorphs are at risk for diabetes. To date, it seems that cavio- morphs produce more insulin than most mammals to compensate for the lower physiologic activity of their insulin.31 This atypical physiologic factor may predispose Dasyprocta to developing diabetes. Feeding captive Dasy- procta as omnivores and feeding a diet low in fermentable carbohydrates seems to be preventative.33 Prevent dental caries: Individuals in wild populations of frugivorous caviomorphs had a 10.5%–19.8% incidence of dental caries.38 This information seems to support that if fed as frugivores, captive Dasyprocta are also at high risk for developing dental caries. Feeding captive Dasyprocta as omnivores and feeding a diet low in fermentable carbohydrates seems to be a preventative.

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